Jeremy B. Caplan

Human theta oscillations exhibit task dependence during virtual maze navigation

Theta oscillations (electroencephalographic activity with a frequency of 4–8 Hz) have long been implicated in spatial navigation in rodents,; however, the role of theta oscillators in human spatial navigation has not been explored. Here we describe subdural recordings from epileptic patients learning to navigate computer-generated mazes. Visual inspection of the raw intracranial signal revealed striking episodes of high-amplitude slow-wave oscillations at a number of areas of the cortex, including temporal cortex. Spectral analysis showed that these oscillations were in the theta band. These episodes of theta activity, which typically last several cycles, are dependent on task characteristics. Theta oscillations occur more frequently in more complex mazes; they are also more frequent during recall trials than during learning trials.

Immediate memory consequences of the effect of emotion on attention to pictures

Emotionally arousing stimuli are at once both highly attention grabbing and memorable. We examined whether emotional enhancement of memory (EEM) reflects an indirect effect of emotion on memory, mediated by enhanced attention to emotional items during encoding. We tested a critical prediction of the mediation hypothesis-that regions conjointly activated by emotion and attention would correlate with subsequent EEM. Participants were scanned with fMRI while they watched emotional or neutral pictures under instructions to attend to them a lot or a little, and were then given an immediate recognition test. A region in the left fusiform gyrus was activated by emotion, voluntary attention, and subsequent EEM. A functional network, different for each attention condition, connected this region and the amygdala, which was associated with emotion and EEM, but not with voluntary attention. These findings support an indirect cortical mediation account of immediate EEM that may complement a direct modulation model.

Learning your way around town: how virtual taxicab drivers learn to use both layout and landmark information

By having subjects drive a virtual taxicab through a computer-rendered town, we examined how landmark and layout information interact during spatial navigation. Subject-drivers searched for passengers, and then attempted to take the most efficient route to the requested destinations (one of several target stores). Experiment 1 demonstrated that subjects rapidly learn to find direct paths from random pickup locations to target stores. Experiment 2 varied the degree to which landmark and layout cues were preserved across two successively learned towns. When spatial layout was preserved, transfer was low if only target stores were altered, and high if both target stores and surrounding buildings were altered, even though in the latter case all local views were changed. This suggests that subjects can rapidly acquire a survey representation based on the spatial layout of the town and independent of local views, but that subjects will rely on local views when present, and are harmed when associations between previously learned landmarks are disrupted. We propose that spatial navigation reflects a hierarchical system in which either layout or landmark information is sufficient for orienting and wayfinding; however, when these types of cues conflict, landmarks are preferentially used.

Associative asymmetry in probed recall of serial lists

For pairs of meaningful items (e.g., words), recall accuracy is nearly identical for forward and backward probes. That is, after studying an A-B pair, subjects can recall Agiven B as well as they can recall B given A(Kahana, 2002). To assess whether this symmetry property is unique to pairs, we investigated the effects of study direction on probed recall of word triples and serial lists. Two experiments revealed a forward-recall advantage in both triples and serial lists. In addition, compound cues produced better recall than did single-item adjacent cues, which, in turn, produced better recall than did remote cues. These findings suggest a discontinuity between the associative processes supporting memory for pairs and those supporting memory for sequences of three or more items.

Theta oscillations reflect a putative neural mechanism for human sensorimotor integration

Hippocampal theta oscillations (3-12 Hz) may reflect a mechanism for sensorimotor integration in rats (Bland BH. Prog Neurobiol 26: 1-54, 1986); however, it is unknown whether cortical theta activity underlies sensorimotor integration in humans. Rather, the mu rhythm (8-12 Hz) is typically found to desynchronize during movement. We measured oscillatory EEG activity for two conditions of an instructed delayed reaching paradigm. Conditions 1 and 2 were designed to differentially manipulate the contribution of the ventral visuomotor stream during the response initiation phase. We tested the hypothesis that theta activity would reflect changes in the relevant sensorimotor network: condition 2 engaged ventral stream mechanisms to a greater extent than condition 1. Theta oscillations were more prevalent during movement initiation and execution than during periods of stillness, consistent with a sensorimotor relevance for theta activity. Furthermore, theta activity was more prevalent at temporal sites in condition 2 than condition 1 during response initiation, suggesting that theta activity is present within the necessary sensorimotor network. Mu activity desynchronized more during condition 2 than condition 1, suggesting mu desynchronization is also specific to the sensorimotor network. In summary, cortical theta synchronization and mu desynchronization may represent broadly applicable rhythmic mechanisms for sensorimotor integration in the human brain.

The roles of EEG oscillations in learning relational information

Rhythmic brain activity has been implicated in learning and memory. Many models implicate theta oscillations (4-8 Hz) specifically in learning of relational information such as pairings and ordered lists. We tested this hypothesis in humans by recording electroencephalographic activity while participants studied nouns organised into pairs or triples for a later cued recall test. If theta is critical in learning structured information, then the amount of theta activity present during study of pairs and triples should covary with subsequent memory performance (accuracy and response times). Multivariate partial least squares analysis revealed three patterns of oscillatory activity associated with task conditions in different ways: a) Within subjects, successful study of pairs but not triples was associated with elevations in oscillations at multiple frequencies including theta, b) Frontal theta oscillations, in conjunction with beta oscillations, covaried with memory performance across subjects for both pairs and triples and c) Right-lateralized gamma oscillations in conjunction with low-frequency oscillations were associated with faster responding at the expense of accuracy across subjects for both pairs and triples. These findings support models that implicate theta oscillations in learning structured information rather than item information alone but similar to prior reports, suggest that theta oscillations explain individual variability better than trial-to-trial variability in behavior.

Right-lateralized brain oscillations in human spatial navigation

During spatial navigation, lesion and functional imaging studies suggest that the right hemisphere has a unique functional role. However, studies of direct human brain recordings have not reported interhemisphere differences in navigation-related oscillatory activity. We investigated this apparent discrepancy using intracranial electroencephalographic recordings from 24 neurosurgical patients playing a virtual taxi driver game. When patients were virtually moving in the game, brain oscillations at various frequencies increased in amplitude compared with periods of virtual stillness. Using log-linear analysis, we analyzed the region and frequency specificities of this pattern and found that neocortical movement-related gamma oscillations (34–54 Hz) were significantly lateralized to the right hemisphere, especially in posterior neocortex. We also observed a similar right lateralization of gamma oscillations related to searching for objects at unknown virtual locations. Thus, our results indicate that gamma oscillations in the right neocortex play a special role in human spatial navigation.

A better oscillation detection method robustly extracts EEG rhythms across brain state changes: The human alpha rhythm as a test case

Oscillatory activity is a principal mode of operation in the brain. Despite an intense resurgence of interest in the mechanisms and functions of brain rhythms, methods for the detection and analysis of oscillatory activity in neurophysiological recordings are still highly variable across studies. We recently proposed a method for detecting oscillatory activity from time series data, which we call the BOSC (Better OSCillation detection) method. This method produces systematic, objective, and consistent results across frequencies, brain regions and tasks. It does so by modeling the functional form of the background spectrum by fitting the empirically observed spectrum at the recording site. This minimizes bias in oscillation detection across frequency, region and task. Here we show that the method is also robust to dramatic changes in state that are known to influence the shape of the power spectrum, namely, the presence versus absence of the alpha rhythm, and can be applied to independent components, which are thought to reflect underlying sources, in addition to individual raw signals. This suggests that the BOSC method is an effective tool for measuring changes in rhythmic activity in the more common research scenario wherein state is unknown.

N400 incongruity effect in an episodic memory task reveals different strategies for handling irrelevant contextual information for Japanese than European Canadians

East Asians/Asian Americans show a greater N400 effect due to semantic incongruity between foreground objects and background contexts than European Americans (Goto, Ando, Huang, Yee, & Lewis, 2010). Using analytic attention instructions, we asked Japanese and European Canadians to judge, and later, remember, target animals that were paired with task-irrelevant original (congruent), or novel (incongruent) contexts. We asked: (1) whether the N400 also shows an episodic incongruity effect, due to retrieved contexts conflicting with later-shown novel contexts; and (2) whether the incongruity effect would be more related to performance for Japanese, who have been shown to have more difficulty ignoring such contextual information. Both groups exhibited episodic incongruity effects on the N400, with Japanese showing more typical N400 topographies. However, incongruent-trial accuracy was related to reduction of N400s only for the Japanese. Thus, we found that the N400 can reflect episodic incongruity which poses a greater challenge to Japanese than European Canadians.

Parallel networks operating across attentional deployment and motion processing: A multi-seed partial least squares fMRI study

Anticipatory deployment of attention may operate through networks of brain areas that modulate the representations of to-be-attended items in advance of their occurrence through top-down control. Luks and Simpson (2004) (Luks, T.L., Simpson, G.V., 2004. Preparatory deployment of attention to motion activates higher order motion-processing brain regions. NeuroImage 22, 1515-1522) found activations in both control areas and sensory areas during anticipatory deployment of attention to visual motion in the absence of stimuli. In the present follow-up analysis, we tested which network activity during anticipatory deployment of attention is functionally connected with task-related network activity during subsequent selective processing of motion stimuli. Following a cue (anticipatory phase), participants monitored a sequence of complex motion stimuli for a target motion pattern (task phase). We analyzed fMR signal using a partial least squares analysis with previously identified cue- and motion-related voxels as seed regions. The method identified two networks that covaried with the activity of seed regions during the cue and motion-stimulus-processing phases of the task. We suggest that the first network, involving ventral intraparietal sulcus, superior parietal lobule and motor areas, is related to anticipatory and sustained visuomotor attention. Operating in parallel to this visuomotor attention network, there is a second network, involving visual occipital areas, frontal areas as well as angular and supramarginal gyri, that may underlie anticipatory and sustained visual attention processes.